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      Variability of mitochondrial ORFans hints at possible differences in the system of doubly uniparental inheritance of mitochondria among families of freshwater mussels (Bivalvia: Unionida)

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          Abstract

          Background

          Supernumerary ORFan genes (i.e., open reading frames without obvious homology to other genes) are present in the mitochondrial genomes of gonochoric freshwater mussels (Bivalvia: Unionida) showing doubly uniparental inheritance (DUI) of mitochondria. DUI is a system in which distinct female-transmitted and male-transmitted mitotypes coexist in a single species. In families Unionidae and Margaritiferidae, the transition from dioecy to hermaphroditism and the loss of DUI appear to be linked, and this event seems to affect the integrity of the ORFan genes. These observations led to the hypothesis that the ORFans have a role in DUI and/or sex determination. Complete mitochondrial genome sequences are however scarce for most families of freshwater mussels, therefore hindering a clear localization of DUI in the various lineages and a comprehensive understanding of the influence of the ORFans on DUI and sexual systems. Therefore, we sequenced and characterized eleven new mitogenomes from poorly sampled freshwater mussel families to gather information on the evolution and variability of the ORFan genes and their protein products.

          Results

          We obtained ten complete plus one almost complete mitogenome sequence from ten representative species (gonochoric and hermaphroditic) of families Margaritiferidae, Hyriidae, Mulleriidae, and Iridinidae. ORFan genes are present only in DUI species from Margaritiferidae and Hyriidae, while non-DUI species from Hyriidae, Iridinidae, and Mulleriidae lack them completely, independently of their sexual system. Comparisons among the proteins translated from the newly characterized ORFans and already known ones provide evidence of conserved structures, as well as family-specific features.

          Conclusions

          The ORFan proteins show a comparable organization of secondary structures among different families of freshwater mussels, which supports a conserved physiological role, but also have distinctive family-specific features. Given this latter observation and the fact that the ORFans can be either highly mutated or completely absent in species that secondarily lost DUI depending on their respective family, we hypothesize that some aspects of the connection among ORFans, sexual systems, and DUI may differ in the various lineages of unionids.

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          Most cited references55

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          TranslatorX: multiple alignment of nucleotide sequences guided by amino acid translations

          We present TranslatorX, a web server designed to align protein-coding nucleotide sequences based on their corresponding amino acid translations. Many comparisons between biological sequences (nucleic acids and proteins) involve the construction of multiple alignments. Alignments represent a statement regarding the homology between individual nucleotides or amino acids within homologous genes. As protein-coding DNA sequences evolve as triplets of nucleotides (codons) and it is known that sequence similarity degrades more rapidly at the DNA than at the amino acid level, alignments are generally more accurate when based on amino acids than on their corresponding nucleotides. TranslatorX novelties include: (i) use of all documented genetic codes and the possibility of assigning different genetic codes for each sequence; (ii) a battery of different multiple alignment programs; (iii) translation of ambiguous codons when possible; (iv) an innovative criterion to clean nucleotide alignments with GBlocks based on protein information; and (v) a rich output, including Jalview-powered graphical visualization of the alignments, codon-based alignments coloured according to the corresponding amino acids, measures of compositional bias and first, second and third codon position specific alignments. The TranslatorX server is freely available at http://translatorx.co.uk.
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            T-Coffee: a web server for the multiple sequence alignment of protein and RNA sequences using structural information and homology extension

            This article introduces a new interface for T-Coffee, a consistency-based multiple sequence alignment program. This interface provides an easy and intuitive access to the most popular functionality of the package. These include the default T-Coffee mode for protein and nucleic acid sequences, the M-Coffee mode that allows combining the output of any other aligners, and template-based modes of T-Coffee that deliver high accuracy alignments while using structural or homology derived templates. These three available template modes are Expresso for the alignment of protein with a known 3D-Structure, R-Coffee to align RNA sequences with conserved secondary structures and PSI-Coffee to accurately align distantly related sequences using homology extension. The new server benefits from recent improvements of the T-Coffee algorithm and can align up to 150 sequences as long as 10 000 residues and is available from both http://www.tcoffee.org and its main mirror http://tcoffee.crg.cat.
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              The MPI bioinformatics Toolkit as an integrative platform for advanced protein sequence and structure analysis

              The MPI Bioinformatics Toolkit (http://toolkit.tuebingen.mpg.de) is an open, interactive web service for comprehensive and collaborative protein bioinformatic analysis. It offers a wide array of interconnected, state-of-the-art bioinformatics tools to experts and non-experts alike, developed both externally (e.g. BLAST+, HMMER3, MUSCLE) and internally (e.g. HHpred, HHblits, PCOILS). While a beta version of the Toolkit was released 10 years ago, the current production-level release has been available since 2008 and has serviced more than 1.6 million external user queries. The usage of the Toolkit has continued to increase linearly over the years, reaching more than 400 000 queries in 2015. In fact, through the breadth of its tools and their tight interconnection, the Toolkit has become an excellent platform for experimental scientists as well as a useful resource for teaching bioinformatic inquiry to students in the life sciences. In this article, we report on the evolution of the Toolkit over the last ten years, focusing on the expansion of the tool repertoire (e.g. CS-BLAST, HHblits) and on infrastructural work needed to remain operative in a changing web environment.
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                Author and article information

                Contributors
                guerra.davide86@yahoo.com
                manuelpmlopeslima@gmail.com
                elsafroufe@gmail.com
                han.gan@deakin.edu.au
                mapaz.ondina@usc.es
                rafaela.amaro@usc.es
                m.klunzinger@gmail.com
                ctcallil@gmail.com
                prie.vincent@gmail.com
                arthur.bogan@naturalsciences.org
                don.stewart@acadiau.ca
                s.breton@umontreal.ca
                Journal
                BMC Evol Biol
                BMC Evol. Biol
                BMC Evolutionary Biology
                BioMed Central (London )
                1471-2148
                19 December 2019
                19 December 2019
                2019
                : 19
                : 229
                Affiliations
                [1 ]ISNI 0000 0001 2292 3357, GRID grid.14848.31, Département de Sciences Biologiques, , Université de Montréal, ; Montréal, QC Canada
                [2 ]ISNI 0000 0001 1503 7226, GRID grid.5808.5, CIBIO/InBIO - Research Center in Biodiversity and Genetic Resources, , University of Porto, ; Campus Agrário de Vairão, Vairão, Portugal
                [3 ]ISNI 0000 0001 1503 7226, GRID grid.5808.5, CIIMAR - Interdisciplinary Centre of Marine and Environmental Research, , University of Porto, ; Matosinhos, Portugal
                [4 ]ISNI 0000 0001 0526 7079, GRID grid.1021.2, Deakin Genomics Centre, School of Life and Environmental Sciences, , Deakin University, ; Geelong, Victoria Australia
                [5 ]ISNI 0000000109410645, GRID grid.11794.3a, Departamento de Zooloxía, Xenética e Antropoloxía Física, Facultade de Veterinaria, , Universidade de Santiago de Compostela, ; Campus de Lugo, Lugo, Spain
                [6 ]BWG Environmental, Brisbane, QLD Australia
                [7 ]ISNI 0000 0000 9848 8286, GRID grid.452917.c, Mollusca, Department of Aquatic Zoology, , Western Australian Museum, ; Welshpool, WA Australia
                [8 ]ISNI 0000 0004 0436 6763, GRID grid.1025.6, School of Veterinary and Biological Sciences, , Murdoch University, ; Perth, WA Australia
                [9 ]ISNI 0000 0001 2322 4953, GRID grid.411206.0, ECOBiv - Ecology and Conservation of Bivalves Research Group, Department of Biology and Zoology, , Federal University of Mato Grosso, ; Cuiabá, MT Brazil
                [10 ]Institut Systématique Evolution Biodiversité ISYEB - Muséum National d’Histoire Naturelle, CNRS, Sorbonne Université, EPHE, Université des Antilles, Paris, France
                [11 ]ISNI 0000 0001 2226 059X, GRID grid.421582.8, North Carolina Museum of Natural Sciences, ; Raleigh, NC USA
                [12 ]ISNI 0000 0004 1936 9633, GRID grid.411959.1, Department of Biology, , Acadia University, ; Wolfville, NS Canada
                Author information
                http://orcid.org/0000-0002-8242-7731
                Article
                1554
                10.1186/s12862-019-1554-5
                6923999
                31856711
                cd7cbcdc-a8b1-404a-b562-18380aa1249b
                © The Author(s). 2019

                Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 3 February 2019
                : 9 December 2019
                Funding
                Funded by: ConBiomics
                Award ID: NORTE-01-0145-FEDER-030286
                Funded by: Natural Sciences and Engineering Research Council of Canada (CA), Discovery Grants
                Award ID: RGPIN/435656-2013
                Award ID: RGPIN/217175-2013
                Award Recipient :
                Funded by: FCT
                Award ID: SFRH/BD/115728/2016
                Award Recipient :
                Funded by: Life+ Margal Ulla
                Award ID: 09NAT/ES/000514
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2019

                Evolutionary Biology
                freshwater mussels,doubly uniparental inheritance of mitochondrial dna,mtdna sequencing,mitochondrial orfan genes,evolution of protein structures and functions,mitochondria and sexual systems

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